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The ring of life provides evidence for a genome fusion origin of eukaryotes

Abstract

Genomes hold within them the record of the evolution of life on Earth. But genome fusions and horizontal gene transfer seem to have obscured sufficiently the gene sequence record such that it is difficult to reconstruct the phylogenetic tree of life. Here we determine the general outline of the tree using complete genome data from representative prokaryotes and eukaryotes and a new genome analysis method that makes it possible to reconstruct ancient genome fusions and phylogenetic trees. Our analyses indicate that the eukaryotic genome resulted from a fusion of two diverse prokaryotic genomes, and therefore at the deepest levels linking prokaryotes and eukaryotes, the tree of life is actually a ring of life. One fusion partner branches from deep within an ancient photosynthetic clade, and the other is related to the archaeal prokaryotes. The eubacterial organism is either a proteobacterium, or a member of a larger photosynthetic clade that includes the Cyanobacteria and the Proteobacteria.

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Figure 1: Conditioned reconstructions provide evidence for the ring of life.
Figure 2: Eubacterial relationships within the ring of life.
Figure 3: A schematic diagram of the ring of life.

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Acknowledgements

We thank A. B. Simonson for helpful discussions and editing, M. Kowalczyk for illustrations, J. Garey for suggesting the original title ‘One ring to rule them all’, and J. A. Servin and R. G. Skophammer for suggestions. This work was supported by grants from the National Science Foundation, NASA Astrobiology Program, The Department of Energy, and the National Institutes of Health to J.A.L.

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Correspondence to James A. Lake.

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Supplementary information

Supplementary Data

This file contains three figures, 13 references, an Introduction and two analysis sections (“Reconstructing the Prokaryotic Tree of Life” and “Assessing whether the choice of conditioning genomes has affected the ring of life?”). (DOC 413 kb)

Supplementary Discussion

This file contains 1 figure and 3 references. It presents a rationale for classifying the tree of life when genome fusions have created new phylogenetic groups. (DOC 47 kb)

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Rivera, M., Lake, J. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155 (2004). https://doi.org/10.1038/nature02848

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